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Virus Surveys in Olive Orchards in Greece Identify Olive Virus T, a Novel Member of the Genus Tepovirus

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Virus Surveys in Olive Orchards in Greece Identify Olive Virus T, a Novel Member of the Genus Tepovirus pathogens Article Virus Surveys in Olive Orchards in Greece Identify Olive Virus T, a Novel Member of the Genus Tepovirus Evanthia Xylogianni 1, Paolo Margaria 2, Dennis Knierim 2, Kyriaki Sareli 1, Stephan Winter 2 and Elisavet K. Chatzivassiliou 1,* 1 Plant Pathology Laboratory, Department of Crop Science, School of Agricultural Production, Infrastructure and Environment, Agricultural University of Athens, Iera Odos 75, Votanikos, 11855 Athens, Greece; [email protected] (E.X.); [email protected] (K.S.) 2 Leibniz-Institute DSMZ-German Collection of Microorganisms and Cell Cultures GmbH, 38124 Braunschweig, Germany; [email protected] (P.M.); [email protected] (D.K.); [email protected] (S.W.) * Correspondence: [email protected]; Tel.: +30-2109-333-207 Abstract: Field surveys were conducted in Greek olive orchards from 2017 to 2020 to collect infor- mation on the sanitary status of the trees. Using a high-throughput sequencing approach, viral sequences were identified in total RNA extracts from several trees and assembled to reconstruct the complete genomes of two isolates of a new viral species of the genus Tepovirus (Betaflexiviridae), for which the name olive virus T (OlVT) is proposed. A reverse transcription–polymerase chain reaction assay was developed which detected OlVT in samples collected in olive growing regions in Central and Northern Greece, showing a virus prevalence of 4.4% in the olive trees screened. Sequences of amplified fragments from the movement–coat protein region of OlVT isolates varied from 75.64% to 99.35%. Three olive varieties (Koroneiki, Arbequina and Frantoio) were infected Citation: Xylogianni, E.; Margaria, P.; with OlVT via grafting to confirm a graft-transmissible agent, but virus infections remained latent. Knierim, D.; Sareli, K.; Winter, S.; In addition, cucumber mosaic virus, olive leaf yellowing-associated virus and cherry leaf roll virus Chatzivassiliou, E.K. Virus Surveys in Olive Orchards in Greece Identify were identified. Olive Virus T, a Novel Member of the Genus Tepovirus. Pathogens 2021, 10, Keywords: phylogenetics; HTS; ArMV; CLRV; CMV; OLYaV; OlVT; SLRSV; TMV; TNV 574. https://doi.org/10.3390/ pathogens10050574 Academic Editor: Akhtar Ali 1. Introduction Olives (Olea europaea L.) have been cultivated in the Mediterranean area since prehis- Received: 30 March 2021 toric times. Greek olive cultivation ranks third in the EU, after Spain and Italy [1], and the Accepted: 5 May 2021 olive agricultural and industrial sector is of immense importance for Greece, providing Published: 8 May 2021 economic, social and environmental services. Olive trees are mainly propagated using semi-hardwood cuttings. This procedure has contributed over the years not only to the dis- Publisher’s Note: MDPI stays neutral semination of the best olive materials, but also to the spread of pathogens, predominantly with regard to jurisdictional claims in viruses. Fifteen viruses have been reported to naturally infect olive trees [2], of which olive published maps and institutional affil- latent virus 1 (OLV-1), olive mild mosaic virus (OMMV) (Alphanecrovirus, Tombusviridae), iations. tobacco necrosis virus D (TNV-D) (Betanecrovirus, Tombusviridae), cucumber mosaic virus (CMV) (Cucumovirus, Bromoviridae), arabis mosaic virus (ArMV), cherry leaf roll virus (CLRV), olive latent ringspot virus (OLRSV) (Nepovirus, Secoviridae), tobacco mosaic virus (TMV) (Tobamovirus, Virgaviridae), olive latent virus 2 (OLV-2) (Oleavirus, Bromoviridae), Copyright: © 2021 by the authors. olive latent virus-3 (OLV-3) (Marafivirus, Tymoviridae), strawberry latent ringspot virus Licensee MDPI, Basel, Switzerland. (SLRSV) (Secoviridae) and olive vein yellowing associated virus (OVYaV) (Closteroviridae) This article is an open access article are officially recognized [3]. In addition, olive yellow mottling and decline associated distributed under the terms and virus (OYMDaV), olive semilatent virus (OSLV) and olive leaf yellowing associated virus conditions of the Creative Commons (OLYaV) have been proposed as distinct, but not yet approved, viral species [3]. In Greece, Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ graft-transmissible, virus-like diseases of olive trees have been reported [4]; however, up- 4.0/). to-date information on the occurrence of viruses in Greek olive orchards is scarce. Only Pathogens 2021, 10, 574. https://doi.org/10.3390/pathogens10050574 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, x FOR PEER REVIEW 2 of 11 Pathogens 2021, 10, 574 2 of 11 however, up-to-date information on the occurrence of viruses in Greek olive orchards is scarce. Only recently, SLRSV, CLRV, OLYaV and ArMV were detected in a germplasm collection of the Greek Institute of Olive Tree, Subtropical Plants and Viticulture (IOSV) recently,in Chania SLRSV, (Crete) CLRV, [5]. In OLYaV earlier and studies ArMV reporting were detected from Greece, in a germplasm only OLV-3 collection was found of the to GreekinfectInstitute olive trees of Olive [6] with Tree, OLV-2 Subtropical infecting Plants Ricinus and Viticulture communis (IOSV)L. [7] and in Chania OMMV (Crete) infecting [5]. Inspinach earlier [8]. studies OLYaV reporting was identified from Greece, in onlyGreek OLV-3 olive wasvarieties found grown to infect in olivea Californian trees [6] withgermplasm OLV-2 infectingcollectionRicinus [9], although communis the originL. [7] andof the OMMV virus remains infecting unclear. spinach [8]. OLYaV was identifiedThis study in is Greek the first olive nationwide varieties grown survey in to a Californianinvestigate germplasmthe presence collection of viruses [9 ],in althoughGreek olive the orchards. origin of theVisual virus inspections remains unclear. during the survey did not reveal trees with con- spicuousThis studysymptoms is the indicating first nationwide viral infection survey and to investigate thus confirmed the presence the health of status viruses of inthe Greektrees. To olive support orchards. the survey, Visual a inspections global analysis during of olive the surveytranscriptomes did not was reveal performed trees with fol- conspicuouslowing a high-throughput symptoms indicating sequencing viral (HTS) infection approach and thus and confirmed subsequently the health a screening status ofby the trees. To support the survey, a global analysis of olive transcriptomes was performed RT–PCR. HTS permitted the discovery of a new viral species assigned to the genus Tepo- following a high-throughput sequencing (HTS) approach and subsequently a screening virus (Betaflexiviridae) for which the name olive virus T (OlVT) is proposed. RT–PCR tests by RT–PCR. HTS permitted the discovery of a new viral species assigned to the genus identified OlVT, CMV, CLRV and OLYaV infection in several olive trees. Tepovirus (Betaflexiviridae) for which the name olive virus T (OlVT) is proposed. RT–PCR tests identified OlVT, CMV, CLRV and OLYaV infection in several olive trees. 2. Results 2.2.1. Results Complete Genome Sequence Determination of a Novel Tepovirus 2.1. CompleteAnalysis Genome of the Sequence RNA-seq Determination data from ofth ae Novelpooled Tepovirus samples and BLAST alignments againstAnalysis a reference of the RNA-seqdatabase datarevealed from the the presence pooled samples of contigs and with BLAST similarity alignments to Tepovirus against amembers, reference databasein particular revealed to the the prunus presence virus of contigsT (PrVT) with isolate similarity Aze239 to [10]Tepovirus in poolmembers, MiV301 in(Table particular S1). No to theother prunus contigs virus with T (PrVT) homology isolate to Aze239viral sequences [10] in pool could MiV301 be identified (Table S1). by NoBLASTn other contigsor BLASTp with alignment. homology Screening to viral sequences of the RNAs could from be the identified samples by composing BLASTn orthe BLASTppool allowed alignment. us to trace Screening an infected of the plant, RNAs co fromrresponding the samples to sample composing GR168, the to pool its collection allowed usin toLamia, trace anFthiotida. infected Following plant, corresponding standard RT–PCR to sample and GR168, 5’-3´RACE to its reactions, collection a in complete Lamia, Fthiotida.genome of Following 6845 nt was standard assembled RT–PCR (isolate and GR168). 5’-3’ RACE The reactions,genome showed a complete an organization genome of 6845typical nt wasof members assembled of the (isolate genus GR168). Tepovirus The (Figure genome 1), showed containing an organizationthree overlapping typical open of membersreading frames of the genus(ORFs)Tepovirus that in direction(Figure1 ),5´ containingto 3´ encode three a replication-associated overlapping open reading protein frames(REP, position (ORFs) that 59–5395 in direction nt; 1778 5’ aa, to 3’ 205.4 encode kDa), a replication-associated a putative movement protein protein (REP, (MP, position position 59–53955307–6458 nt; nt; 1778 383 aa, aa, 205.4 42.6 kDa),kDa) and a putative a capsid movement protein (CP, protein position (MP, 6106–6771 position 5307–6458 nt; 221 aa, nt;25.2 383 kDa). aa, 42.6Two kDa) non-coding and a capsid regions protein (UTR) (CP, of 58 position nt and 6106–677174 nt in length nt; 221 are aa,present 25.2 kDa).at the Two5´and non-coding 3´ ends of regions the genome, (UTR) respectively. of 58 nt and As 74 ntfor inother length members are present of the at Betaflexiviridae the 5’ and 3’ endsfamily, of thea polyA genome, tail respectively.follows the 3´ As UTR. for otherPrediction members of conserved of the Betaflexiviridae domains
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